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Aspects of Natural Cold Tolerance in Ectothermic Animals

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Aspects of Natural Cold Tolerance in Ectothermic Animals Human Reproduction Vol. 15, (Suppl. 5) pp. 26-46, 2000 Aspects of natural cold tolerance in ectothermic animals Hans Raml0y Department of Life Sciences and Chemistry, Roskilde University, P.O.Box 260, DK 4000 Roskilde, Denmark Downloaded from https://academic.oup.com/humrep/article/15/suppl_5/26/554993 by guest on 24 September 2021 E-mail: [email protected] Polar, alpine and temperate ectothermic (cold- Key words: antifreeze protein/cold tolerance/cryo- blooded) animals encounter temperatures below protectant/ice-nucleating agent/membrane the melting point of their body fluids either diurnally or seasonally. These animals have developed a number of biochemical and physio- Introduction logical adaptations to survive the low temper- Animals living in polar, temperate and alpine atures. The problems posed to the animals environments are either on a daily or yearly basis during cold periods include changes in mem- subjected to temperatures well below the freezing brane and protein structure due to phase point of their body fluids. Liquid water is necessary changes in these molecules, changes in electro- for all life processes, therefore these animals must lyte concentrations and other solutes in the body either avoid freezing of body fluids but survive fluids as well as changes in metabolism. Cold- the low temperatures or be able to endure ice tolerant ectothermic animals can be divided into formation in body fluids. A number of such animals two groups depending which of two 'strategies' are endothermic and survive the low temperatures they employ to survive the low temperatures: by way of insulation such as fur or fat. The freeze-tolerant animals which survive ice forma- ectothermic (cold-blooded) animals, in which body tion in the tissues and freeze-avoiding animals temperature follows the surrounding environment, which tolerate the low temperatures but not have a number of options when the temperature crystallization of the body fluids. The adapta- falls: they can hide in microhabitats where they tions are mainly directed towards the control are not exposed to low temperatures; they can or avoidance of ice formation and include the leave the area and return when conditions become synthesis of low mol. wt cryoprotectants, ice- more hospitable; or they can adapt to the low nucleating agents and antifreeze proteins. How- temperatures via a number of morphological, ana- ever, some of the adaptations such as the syn- tomical, biochemical and physiological features. thesis of low mol. wt cryoprotectants are also The present review focuses on this last group of more specific in their mechanism, e.g. direct animals and their biochemical and physiological stabilizing interaction with membranes and pro- adaptations. In view of the temperature sensitivity teins. The mechanisms employed by such of mammalian gametes and embryos, important clues to the potential effects of cold and their animals may offer ideas and information on avoidance may be gained from comparative studies. alternative approaches which might be usefully employed in the cryopreservation of cells and Damages due to cold per se tissues frequently required in assisted repro- Animals living in areas where they are exposed to ductive technology. low temperatures, or temperatures that are lower 26 © European Society of Human Reproduction and Embryology Cold tolerance in ectotherms than the temperature at which the animals are membrane function requires the liquid crystalline normally active, may suffer damage due to the phase, in which the membrane is strain-free, so cold per se. The temperature does not need to fall that hydrophobic regions of proteins and the lipid below the melting point of the body fluids to cause bilayer can be matched (Bloom, 1998). It should damage. Damage caused by the cold per se is be noted that if the hydration of the membrane due to either changes in metabolism or to phase changes, the lipids may go through the liquid transitions in membranes and proteins as a result crystalline to gel transition and even reach a phase Downloaded from https://academic.oup.com/humrep/article/15/suppl_5/26/554993 by guest on 24 September 2021 of the low temperatures. called the hexagonal II (Hn) phase, where the lipids organize into a non-lamellar three-dimen- Phase changes in membranes sional matrix with the hydrophilic headgroups Biological membranes are bilayers of 20-80% pointing inwards towards 'channels' of water while lipids, mostly phosphoglycerides, with one primary the hydrophobic hydrocarbon chains are pointing hydroxyl group esterified to phosphoric acid and towards each other (Quinn, 1985). the other hydroxyl groups esterified to fatty acids. Biological membranes are not composed of only The phosphoglycerides also contain a polar head one pure lipid but rather of many—up to 200 group often in the form of an amino alcohol, which different lipids are found in the membranes of is esterified to the phosphoric acid via its hydroxyl some biological systems (Morris and Clarke, 1987). group. This arrangement gives rise to amphipathic Differential calorimetric studies have shown that compounds or 'polar lipids', because of their polar a mixture of a saturated and a non-saturated lipid headgroups and their non-polar hydrocarbon tails gives rise to two distinct endotherms if the mixture consisting of 16, 18, 20 or 22 carbon atoms is heated from below the liquid-crystalline phase (Lehninger, 1975; Grout and Morris, 1987). The temperature (Tc) for both lipids to a temperature bilayers are formed as a consequence of the amphi- above the Tc for both lipids. These endotherms pathic nature of the phospholipids. In the presence arise from the phase transitions of laterally phase- of water the hydrophilic headgroups are exposed separated domains of the unsaturated and saturated to the water and the hydrophobic hydrocarbon lipids respectively. The two lipids were separated chains form the core of the membrane. The integrity into domains that consisted of the pure lipid of of the biological membrane is determined by one or the other. The saturated lipids stayed in several factors such as Van der Waals forces the gel phase at a higher temperature than the (electrostatic interactions), salt bridges, hydrogen unsaturated lipids but on further heating these also bonds and, perhaps more importantly, thermodyn- underwent a phase transition and entered the liquid amic relations such as hydrophobic interaction and crystalline phase (Quinn, 1985; Gennis, 1989). entropy. The hydrogen bonding of numerous water Chapman et al. (1977) have proposed a model for molecules to each other is one of the strongest the occurrences in the biological membrane during forces driving the membrane into its lamellar cooling. They suggest that cooling a biological configuration (van Oss and Good, 1996). Mem- membrane below the Tc of the lipids leads to lateral brane structure is dependent on temperature, pH, phase separations and that it also has profound ionic strength of the surrounding medium and the effects on the distribution of the proteins bound state of hydration (Williams, 1990). to or integrated into the membrane. When the During cooling, the initial effect is an increase membrane is cooled, some lipids function as 'nuc- in membrane viscosity (Grout and Morris, 1987). leation sites' and undergo a phase transition, crys- Upon further cooling, phase separations are likely tallizing into 'islands' of the gel phase in which to occur. A characteristic of bilayers of a pure lipid proteins become trapped. Along the edges of these is the phase transition temperature (Tc) above 'islands' packing faults are likely and as the which the lipid bilayers are found in a disordered proximity of the proteins increases these may begin phase called the liquid crystalline state and below to aggregate (Quinn, 1985). which the bilayer is found in the more ordered The consequences of the thermotropic behaviour gel state (Morris and Clarke, 1987). Efficient of membrane lipids are diverse. A number of the 27 H.Raml0v membrane components are free to diffuse within exposure to low temperature is imperative if the the membrane. Phase separations and the increase biological system is to survive. in membrane viscosity will have effects on the According to Franks and Hadley (1992), the kinetics of diffusion-controlled processes (Grout cold denaturation temperatures of most proteins and Morris, 1987). Enzymes associated with the when examined in the pH range of maximal membranes may become clustered into small stability lie below the equilibrium freezing point domains of liquid lipid and this may have various of water. For the majority of the examined proteins effects on membrane function; there may be an this means below -15°C. The stability of proteins Downloaded from https://academic.oup.com/humrep/article/15/suppl_5/26/554993 by guest on 24 September 2021 increased probability of the enzymes getting into in solution is very limited (Franks, 1985) and contact with their substrates which may lead to presumably based on a number of contributing increased enzyme activity (Grout and Morris, factors, which can be divided into stabilizing and 1987). In contrast, such an aggregation of the destabilizing factors. The former are hydrophobic enzymes could also impede the transport of various interactions, intrapeptide attractive effects (hydro- molecules across the membrane, e.g. where gen bonding, salt bridges, van der Waals inter- aggregations of enzymes may deplete an area of actions) whilst the latter are core repulsion, substrate in the immediate vicinity of the enzymes. configurational entropy and solvation effects Here, transportation rates would decrease and (Franks and Hadley, 1992). The increasing magni- depend upon the diffusion of new substrate to the tude of the latter, particularly solvation of non-polar enzyme aggregation in question. (hydrophobic) moieties upon cooling, is thought to The boundaries between the gel phase and the be the molecular origin of cold denaturation (Hvidt liquid-crystalline phase are known to be especially and Westh, 1998). Denaturation of proteins at low leaky (Williams, 1990).
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